Viral hemorrhagic septicemia

VHS disease in a gizzard shad

Viral hemorrhagic septicemia (VHS) is a deadly infectious fish disease caused by Viral hemorrhagic septicemia virus. It afflicts over 50 species of freshwater and marine fish in several parts of the Northern Hemisphere.[1] Different strains of the virus occur in different regions, and affect different species. There are no signs that the disease affects human health. VHS is also known as Egtved disease, and the virus as Egtved virus.[2]

Historically, VHS was associated mostly with freshwater salmonids in western Europe, documented as a pathogenic disease among cultured salmonids since the 1950s.[3] Today it is still a major concern for many fish farms in Europe and is therefore being watched closely by the European Community Reference Laboratory for Fish Diseases. It was first discovered in the US in 1988 among salmon returning from the Pacific in Washington state.[4] This North American genotype was identified as a distinct, more marine-stable strain than the European genotype. VHS has since been found afflicting marine fish in the northeastern Pacific Ocean, the North Sea, and the Baltic Sea.[3] Since 2005, massive die-offs have occurred among a wide variety of freshwater species in the Great Lakes region of North America.

Virus taxonomy

[edit]
Piscine novirhabdovirus
Negative stain electron micrograph of "Piscine novirhabdovirus"
Negative stain electron micrograph of Piscine novirhabdovirus
Virus classification Edit this classification
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Negarnaviricota
Class: Monjiviricetes
Order: Mononegavirales
Family: Rhabdoviridae
Genus: Novirhabdovirus
Species:
Piscine novirhabdovirus
Synonyms
  • Egtved virus[2]
  • Oncorhynchus 2 novirhabdovirus[5]
  • Viral hemorrhagic septicemia virus[6]

VHSV is a negative-sense single-stranded RNA virus of the order Mononegavirales, family Rhabdoviridae, and genus Novirhabdovirus.[7] Another related fish rhabdovirus in the genus Novirhabdovirus is Salmonid novirhabdovirus (formerly Infectious hematopoietic necrosis virus (IHNV)), which causes infectious hematopoietic necrosis (IHN) disease in salmonidae.

The viral cause of the disease was discovered in 1963 by M. H. Jenson.[8] The virus is an enveloped, bullet-shaped particle, about 180 nm long by 60 nm in diameter, covered with 5 to 15 nm long peplomers.[2]

Molecular virology

[edit]

The genome of VHSV is composed of approximately 11 kb of single stranded RNA, which contains six genes that are located along the genome in the 3′–5′ order: 3′-N-P-M-G-NV-L-5′, nucleocapsid protein (N), polymerase-associated phosphoprotein (P), matrix protein (M), surface glycoprotein (G), a unique non-virion protein (NV), and virus polymerase (L).

VHSV enters the host cell through either fusion or endocytosis. It binds to a glycoprotein, called fibronectin, in the extracellular matrix. VHSV does its binding through integrin receptors.[9]

Reverse genetics is a powerful tool to study and characterize the previously unknown viral genes. Reverse genetics system is currently available for VHSV.[10][11] A vaccinia virus free reverse genetic system for Great Lakes VHSV (Genotype IVb) was developed by a research group from the USA.[11] This system allows the investigators to explore the functional properties of individual viral genes of VHSV in detail. This system was immediately utilized to characterize the non-virion (NV) gene of novirhabdoviruses. Even though it has been demonstrated that the NV gene is not necessary for viral replication, it is highly essential for viral pathogenesis. A new role of NV protein has been discovered and demonstrated that it inhibits apoptosis at the early stage of viral infection.[12] This discovery unlocked the mystery of presence of NV proteins in novirhabdoviruses.

Virus subtypes

[edit]

Different isolates (unique strains) of VHSV are typically grouped by genotyping. It is found that genotype groups are divided more geographically than by host species. Earlier studies used different numbering systems,[13][14] but the following system has come into common usage based on genotype similarity based on sequencing of the N- and G-genes. Types I-III are enzootic to Europe, and Type IV to North America, and Type I and type IV isolates are further subdivided, as follows:

Type Prevalent host type and location
  I-a Farmed rainbow trout and a few other freshwater fish in continental Europe[15]
  I-b Marine fish of the Baltic Sea, Skagerrak, Kattegat, North Sea, Japan[1]
  I-c Farmed rainbow trout Denmark
  I-d Farmed rainbow trout in Norway, Finland, Gulf of Bothnia
  I-e Rainbow trout in Georgia, farmed and wild turbot in the Black Sea[16]
  II Marine fish of the Baltic Sea
  III Marine fish of the British Isles and northern France, farmed turbot in the UK and Ireland, and Greenland halibut (Reinhardtius hippoglossoides) in Greenland.[17] Farmed rainbow trout in Norway.[18]
  IV-a Marine fish of the Northwest Pacific (North America), North American north Atlantic coast,[19] Japan, and Korea[1][20]
  IV-b Freshwater fish in North American Great Lakes region[20]

Type I-a was the only strain known from VHSV's discovery in 1963 until the late 1988, isolated to fish farms in continental Europe, affecting primarily rainbow trout and occasionally brown trout or pike.[21]

In 1988, the first marine strain of VHSV, now designated type IV, was found in normal-appearing salmon returning from the Pacific to rivers of Washington State. This strain and other marine strains were not lethal to rainbow trout. The discovery prompted further studies, and by the mid-1990s, marine VHSV was found in eight species along the northern North America's Pacific coast, and 14 species in and around the Atlantic's North Sea.[22] 1996 saw the first VHSV in Japan, among Japanese flounder farmed in the Seto Inland Sea,[23] and different genotypes have appeared in different areas since then.[13] Type IV was later found off North America's northern Atlantic coast, in Atlantic herring (Clupea harengus)[24] mummichog (Fundulus heteroclitus), stickleback (Gasterosteus aculeatus aculeatus), brown trout (Salmo trutta), and striped bass (Morone saxatilis),[17] as well as dozens of freshwater species in the Great Lakes.

VHSV continues to be found in new geographical areas, in new species of fish. This is thought to represent both the spread of the virus into new areas, as with VHSV egg and live fish transfers from North America to Asia, or feeding of raw marine fish to inland farmed trout in Finland,[15] as well as discovery of existing populations, as with an apparently well established marine reservoir in the Black Sea.[16]

To keep track of the distribution of different VHSV genotypes, a database called Fishpathogens.eu[25] has been created to store data on different fish pathogens (including VHSV) and their sequences.

Evolution

[edit]

This virus appears to have evolved in the Pacific Northwest of North America.[26] It appears to have diverged into several strains ~300 years ago.

Great Lakes Type IV-b

[edit]

The Type IV-b strain of VHSV has been spreading among freshwater fish in the Great Lakes region since at least 2003, resulting in some massive die-offs since 2005 of many species in the affected lakes.[1] Originally found off the Atlantic coast of Canada, it was considered a low mortality marine strain. Its first detection in freshwater was in Lake Ontario in 2005, and then in an archived 2003 sample from Lake St. Clair.[27] The isolate was named MI03GL and was sequenced for its entire genome.[28]

The North American genotype of the virus, in addition to moderate mortality to salmonid species, including various varieties of trout, is also proving virulent among a wide variety of warm-water species previously considered resistant to VHS. The Great Lakes region variant has killed lake trout, steelhead trout, chinook salmon, yellow perch, gobies, emerald shiners, muskies, whitefish, and walleye. While the European strain of VHSV is particularly deadly to rainbow trout, the Great Lakes region variant affects the species only mildly, as is typical with primarily marine genotypes.

Great Lakes regional distribution

[edit]

An archived 2003 sample from Lake St. Clair of Great Lakes muskellunge is the earliest confirmed case of VHSV within the Great Lakes region.[20] Lake St. Clair connects to Lake Erie through the Detroit River to the south, and to Lake Huron through the St. Clair River to the north. The sample was not tested for VHS until 2005, after the disease was detected in Lake Ontario.[27]

2005 samples of Lake Ontario freshwater drum and Lake Huron lake whitefish were infected with VHS. Initially classified as an unknown rhabdovirus, the Lake Ontario sample was confirmed to be VHSV in 2006, while the Lake Huron sample was confirmed to be VHSV in 2007.[20]

2006 saw mass die-offs from VHS in Lake Erie, the St. Clair River, the Detroit River, and the St. Lawrence River, which connects the Great Lakes to the Atlantic Ocean.[20] VHS was further detected in the Niagara River, which connects Lake Erie to Lake Ontario.[29] It was also found in a walleye die-off in the landlocked inland Conesus Lake, the westernmost of the Finger Lakes in western New York state.[30] This was the first case in the region outside waters contiguously connected to the Great Lakes.

On May 12, 2007, the Wisconsin DNR announced the likely presence of VHS in Wisconsin's inland Little Lake Butte des Morts. Preliminary tests of samples of freshwater drum collected on May 2 were positive, and the announcement came amidst a die-off of hundreds of freshwater drum there and on neighboring Lake Winnebago.[31] Preliminary tests later indicated VHS in specimens from Lake Winnebago.[32] The lakes drain through the Fox River to Lake Michigan's Green Bay.

On May 17, 2007, the Michigan DNR confirmed the presence of VHS in the Michigan's inland Budd Lake, a popular fishing destination is in the central part of Michigan's lower peninsula.[33] A major die-off of VHS-positive muskies, bluegills, and black crappie began on April 30, 2007.[34]

On May 24, 2007, preliminary tests indicated the presence of VHS in a brown trout from Lake Michigan, the second largest freshwater lake in the United States. Contamination in the lake had been expected for months by experts, since the presence of VHS was confirmed in the connected Lake Huron.[35]

On July 14, 2007, federal labs confirmed the presence of VHS in Skaneateles Lake, the second of New York's Finger Lakes to test positive for the disease.[36] The disease caused a large die-off of bass in the spring of 2007.

Government regulation

[edit]

Before the Type IVb die-offs in the Great Lakes, few states regulated transfer of live species other than for salmonids. Since 2005, new policies have been adopted concerning fish and egg transfer, use of live bait, and water transfer, aimed at curtailing the spread to new lakes and rivers in the region. As of July 13, 2007, new rules have been enacted in the Canadian province of Ontario,[37] and US states of Michigan, New York, Ohio, Pennsylvania, and Wisconsin, while they are currently being drafted in Illinois, Indiana, and Minnesota.[38] Additionally, the USDA's Animal and Plant Health Inspection Service issued a federal order in the fall of 2006 barring the transfer of all live susceptible species from the eight states bordering the lower Great Lakes, as well as importing such species from the Canadian provinces of Ontario and Quebec.[39][40]

Transmission

[edit]

VHSV can be spread from fish to fish through water transfer, as well as through contaminated eggs,[3] and bait fish from infected waters.[8] The emerald shiner is a particularly popular bait fish in the Great Lakes region, and is among the species afflicted.[41]

Survivors of the disease can become lifelong carriers of the virus, contaminating water with urine, sperm, and ovarian fluids.[1] The virus has been shown to survive two freeze/thaw cycles in a conventional freezer, suggesting both live and frozen bait could be a transmission vector. In Europe, the gray heron has spread the virus, but it does so mechanically; the virus is apparently inactive in the digestive tract of birds.[2]

Symptoms

[edit]

Fish that become infected experience hemorrhaging of their internal organs, skin, and muscle. Some fish show no external symptoms, but others show signs of infection that include bulging eyes, bloated abdomens, bruised-looking reddish tints to the eyes, skin, gills and fins. Some infected fish have open sores that may look like the lesions from other diseases or from lamprey attacks.[42]

There may also be a nervous form of the disease where fish are constantly flashing and showing abnormal behaviour.[43]

Diagnosis

[edit]

Field diagnosis

[edit]

Living fish afflicted with VHS may appear listless or limp, hang just beneath the surface, or swim very abnormally, such as constant flashing circling due to the tropism of the virus for the brain.

External signs may include darker coloration, exophthalmia ("pop eye"), pale or red-dotted gills, sunken eyes, and bleeding around orbits (eye sockets) and at base of fins.[20][21][44]

Genetics researchers at the Lake Erie Research Center at the University of Toledo are developing a test[45] that will speed diagnosis from a month to a matter of hours.

Gross pathology (non-laboratory)

[edit]

VHSV is a hemorrhagic disease, meaning it causes bleeding. Internally, the virus can cause petechial hemorrhaging (tiny spots of blood) in internal muscle tissue, and petechial or severe hemorrhaging in internal organs and other tissues. Internal hemorrhaging can be observed as red spots inside a dead fish, particularly around the kidney, spleen, and intestines, as well as the swim bladder, which would normally have a clear membrane. The liver may be pale, mottled with red hyperemic areas, the kidney may be swollen and unusually red, the spleen may be swollen, and the digestive tract may be empty.[21]

External signs are not always present, but if they are, hemorrhaging on the skin's surface can appear as anywhere from tiny red dots (petechiae) to large red patches.

Histopathology (microscopic tissue analysis)

[edit]

Preliminary diagnosis involves histopathological examination, observing tissues through a microscope. Most tissue changes can be observed as minor to major necrosis (cell death) in the liver, kidneys, spleen, and skeletal muscle. The hematopoietic (blood-forming) areas of the kidney and spleen are the initial area of infection, and should show necrosis. The gill may have thickened lamellae, and the liver may have pyknotic nuclei. Skeletal muscle accumulates blood but does not suffer much damage.[21]

Virology (definitive testing)

[edit]

Electron microscopy can reveal the bullet-shaped rhabdovirus, but is not adequate for definitive diagnosis.

The Manual or Diagnostic for Aquatic Animals, 2006, is the standard reference for definitive tests. In most cases, cell culturization is recommended for surveillance, with antibody tests and reverse transcription polymerase chain reaction (RT-PCR) and genetic sequencing and comparison for definitive confirmation and genotype classification.[21][44]

Virus neutralisation is another important method of diagnosis, especially for carrier fish.

Prevention

[edit]

Thoroughly cleaning boats, trailers, nets and other equipment when traveling between different lakes and streams also helps. The only EPA-approved disinfectant proven effective against VHS is Virkon AQUATIC).[46] Chlorine bleach kills the VHS virus, but in concentrations that are much too caustic for ordinary use. Disinfecting stations can be found at various inland lake boat launches in the Great Lakes region.

Immune reactions against VHSV

[edit]

Fish viperin gene was identified as an interferon-stimulated gene against VHSV. Whereas, viperin produces inhibitory ddhCTP (3ʹ-deoxy-3′,4ʹdidehydro-CTP), which is an elongation inhibitor. Thereby, the VHSV RNA replication is terminated.[47] [48]

References

[edit]
  1. ^ a b c d e Rovid-Spickler A (17 May 2007). "Disease Factsheets: Viral Hemorrhagic Septicemia" (PDF). The Center for Food Security & Public Health. Iowa State University. Retrieved 12 July 2007.
  2. ^ a b c d McAllister PE (1990). "Viral Hemorrhagic Septicemia of Fishes". Fish Disease Leaflet. United States Department of the Interior, U.S. Fish and Wildlife Service. Archived from the original on 15 June 2007. Retrieved 12 July 2007.
  3. ^ a b c "Description of Viruses: Family Rhabdoviridae, Genus Novirhabdovirus". Virus Taxonomy Online: Seventh Report of the International Committee on Taxonomy of Viruses. 2000. Archived from the original on 27 September 2007. Retrieved 12 July 2007.
  4. ^ Meyers TR, Sullivan J, Emmenegger E, Follett J, Short S, Batts WN (1992). "Identification of viral hemorrhagic septicemia virus isolated from Pacific cod Gadus macrocephalus in Prince William Sound, Alaska, USA". Diseases of Aquatic Organisms. 12: 167–75. doi:10.3354/dao012167.
  5. ^ Kurath G, Kuhn JH (18 July 2016). "Rename two (2) species in the genus Novirhabdovirus" (PDF). International Committee on Taxonomy of Viruses (ICTV). Retrieved 15 June 2019.
  6. ^ Walker P (15 June 2015). "Implementation of taxon-wide non-Latinized binomial species names in the family Rhabdoviridae" (PDF). International Committee on Taxonomy of Viruses (ICTV). p. 7. Retrieved 15 June 2019.
  7. ^ "Viral hemorrhagic septicemia virus". NCBI Taxonomy Database. United States Department of Health and Human Services, National Institutes of Health, National Library of Medicine, National Center for Biotechnology Information. Retrieved 14 July 2007.
  8. ^ a b Kipp RM, Ricciardi A (8 December 2006). Viral Hemorrhagic Septicemia (VHS) (PDF). VHS Factsheet (Report). Great Lakes Aquatic Nonindigenous Species Information System (GLANSIS). Retrieved 16 July 2007.
  9. ^ Nombela I, Puente-Marin S, Chico V, Villena AJ, Carracedo B, Ciordia S, et al. (2018-02-09). "Identification of diverse defense mechanisms in rainbow trout red blood cells in response to halted replication of VHS virus". F1000Research. 6: 1958. doi:10.12688/f1000research.12985.2. PMC 5820608. PMID 29527292.
  10. ^ Biacchesi S, Lamoureux A, Mérour E, Bernard J, Brémont M (October 2010). "Limited interference at the early stage of infection between two recombinant novirhabdoviruses: viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus". Journal of Virology. 84 (19): 10038–10050. doi:10.1128/JVI.00343-10. PMC 2937753. PMID 20631140.
  11. ^ a b Ammayappan A, Kurath G, Thompson TM, Vakharia VN (August 2011). "A reverse genetics system for the Great Lakes strain of viral hemorrhagic septicemia virus: the NV gene is required for pathogenicity". Marine Biotechnology. 13 (4): 672–683. Bibcode:2011MarBt..13..672A. doi:10.1007/s10126-010-9329-4. PMID 20936318. S2CID 24597813.
  12. ^ Ammayappan A, Vakharia VN (August 2011). "Nonvirion protein of novirhabdovirus suppresses apoptosis at the early stage of virus infection". Journal of Virology. 85 (16): 8393–8402. doi:10.1128/JVI.00597-11. PMC 3147959. PMID 21653667.
  13. ^ a b Nishizawa T, Iida H, Takano R, Isshiki T, Nakajima K, Muroga K (March 2002). "Genetic relatedness among Japanese, American and European isolates of viral hemorrhagic septicemia virus (VHSV) based on partial G and P genes". Diseases of Aquatic Organisms. 48 (2): 143–148. doi:10.3354/dao048143. PMID 12005236.
  14. ^ Thiéry R, de Boisséson C, Jeffroy J, Castric J, de Kinkelin P, Benmansour A (November 2002). "Phylogenetic analysis of viral haemorrhagic septicaemia virus (VHSV) isolates from France (1971-1999)". Diseases of Aquatic Organisms. 52 (1): 29–37. doi:10.3354/dao052029. PMID 12517003.
  15. ^ a b Einer-Jensen K, Ahrens P, Forsberg R, Lorenzen N (May 2004). "Evolution of the fish rhabdovirus viral haemorrhagic septicaemia virus". The Journal of General Virology. 85 (Pt 5): 1167–1179. doi:10.1099/vir.0.79820-0. PMID 15105533.
  16. ^ a b Nishizawa T, Savas H, Isidan H, Ustündağ C, Iwamoto H, Yoshimizu M (April 2006). "Genotyping and pathogenicity of viral hemorrhagic septicemia virus from free-living turbot (Psetta maxima) in a Turkish coastal area of the Black Sea". Applied and Environmental Microbiology. 72 (4): 2373–2378. Bibcode:2006ApEnM..72.2373N. doi:10.1128/AEM.72.4.2373-2378.2006. PMC 1449023. PMID 16597932.
  17. ^ a b Gagné N, Mackinnon AM, Boston L, Souter B, Cook-Versloot M, Griffiths S, Olivier G (April 2007). "Isolation of viral haemorrhagic septicaemia virus from mummichog, stickleback, striped bass and brown trout in eastern Canada". Journal of Fish Diseases. 30 (4): 213–223. Bibcode:2007JFDis..30..213G. doi:10.1111/j.1365-2761.2007.00802.x. PMID 17394523.
  18. ^ Dale OB, Ørpetveit I, Lyngstad TM, Kahns S, Skall HF, Olesen NJ, Dannevig BH (June 2009). "Outbreak of viral haemorrhagic septicaemia (VHS) in seawater-farmed rainbow trout in Norway caused by VHS virus Genotype III". Diseases of Aquatic Organisms. 85 (2): 93–103. doi:10.3354/dao02065. PMID 19694169.
  19. ^ Report of the ICES Advisory Committee on Fishery Management, Advisory Committee on the Marine Environment and Advisory Committee on Ecosystems, 2006. Book 2 (PDF). Copenhagen: International Council for the Exploration of the Sea. 2006. ISBN 87-7482-053-2. Archived from the original (PDF) on 31 October 2007.
  20. ^ a b c d e f Whelan GE (26 February 2007). "Viral Hemorrhagic Septicemia (VHS) Briefing Paper" (PDF). Michigan Department of Natural Resources. Archived from the original (PDF) on 17 February 2007. Retrieved 13 July 2007.
  21. ^ a b c d e Crane M (2006). "Chapter 2.1.5: Viral Hemorrhagic Septicaemia". Manual of Diagnostic Tests for Aquatic animals. Archived from the original on 6 February 2007. Retrieved 16 July 2007.
  22. ^ Importation of pilchards (Sardinops sagax) for direct introduction into natural waters: Biosecurity policy review of viral haemorrhagic septicaemia virus (VHSV), Draft Report. Department of Agriculture Fisheries and Forestry (Report). Commonwealth of Australia. June 2003. Archived from the original on 27 September 2007. Retrieved 16 July 2007.
  23. ^ Isshik T, Nishizawa T, Kobayashi T, Nagano T, Miyazaki T (November 2001). "An outbreak of VHSV (viral hemorrhagic septicemia virus) infection in farmed Japanese flounder Paralichthys olivaceus in Japan". Diseases of Aquatic Organisms. 47 (2): 87–99. doi:10.3354/dao047087. PMID 11775799.
  24. ^ Elsayed E, Faisal M, Thomas M, Whelan G, Batts W, Winton J (October 2006). "Isolation of viral haemorrhagic septicaemia virus from muskellunge, Esox masquinongy (Mitchill), in Lake St Clair, Michigan, USA reveals a new sublineage of the North American genotype". Journal of Fish Diseases. 29 (10): 611–619. Bibcode:2006JFDis..29..611E. doi:10.1111/j.1365-2761.2006.00755.x. PMID 17026670.
  25. ^ "European Union Reference Laboratory for Fish Diseases Fish Pathogens Database".
  26. ^ He M, Yan XC, Liang Y, Sun XW, Teng CB (August 2014). "Evolution of the viral hemorrhagic septicemia virus: divergence, selection and origin". Molecular Phylogenetics and Evolution. 77: 34–40. Bibcode:2014MolPE..77...34H. doi:10.1016/j.ympev.2014.04.002. PMID 24727199.
  27. ^ a b "Economic impacts of private sector aquaculture-based recreational fishing in the western USA". CSU Research Proposal. Colorado Aquaculture Association. Archived from the original on 3 February 2007. Retrieved 12 July 2007.
  28. ^ Ammayappan A, Vakharia VN (October 2009). "Molecular characterization of the Great Lakes viral hemorrhagic septicemia virus (VHSV) isolate from USA". Virology Journal. 6: 171. doi:10.1186/1743-422X-6-171. PMC 2771013. PMID 19852863.
  29. ^ "Viral Hemorrhagic Septicemia in New York State". Highlights. Cornell University, College of Veterinary Medicine, Department of Microbiology and Immunology, Aquatic Animal Health Program. Archived from the original on 10 June 2007. Retrieved 14 July 2007.
  30. ^ "Viral Hemorrhagic Septicemia (VHS) in New York". New York State Department of Environmental Conservation. Archived from the original on 6 July 2007. Retrieved 14 July 2007.
  31. ^ "Fish likely infected with deadly virus found in Little Lake Butte des Morts; Menasha Lock closed; Public asked to take steps to stop the spread". Wisconsin Department of Natural Resources (Press release). 12 May 2007. Archived from the original on 24 June 2007. Retrieved 13 July 2007.
  32. ^ "Lake Winnebago Fish Preliminarily Test Positive for VHS]. (News release)". Wisconsin Department of Natural Resources. 18 May 2007. Archived from the original on 25 June 2007. Retrieved 13 July 2007.
  33. ^ Barta J. "Michigan's Best Bets for Muskies". Michigan Sportsman. Archived from the original on 27 February 2009. Retrieved 15 July 2007.
  34. ^ "Fish Disease Discovered in Budd Lake, Clare County". Michigan Department of Natural Resources. 17 May 2007. Archived from the original on 14 December 2008. Retrieved 15 July 2007.
  35. ^ "Trout from Lake Michigan likely VHS positive]. (News release)". Wisconsin Department of Natural Resources. 24 May 2007. Archived from the original on 6 August 2007. Retrieved 13 July 2007.
  36. ^ Figura D (14 July 2007). "Federal Lab Confirms VHS Caused Fish Kill". The Post-Standard. Archived from the original on 12 October 2007. Retrieved 15 July 2007.
  37. ^ "Ontario Government Acting Swiftly to Control Further Spread of New Fish Virus]. (Press release)". Ontario Ministry of Natural Resources. 8 January 2007. Archived from the original on 8 February 2007. Retrieved 15 July 2007.
  38. ^ Sander L (13 July 2007). "Michigan's Summer Fishing Turns Less Carefree". The New York Times. Retrieved 13 July 2007.
  39. ^ Gustafson L (April 2007). "VHS Surveillance Planning Under Way" (PDF). NAHSS Outlook. Archived from the original (PDF) on 20 August 2007. Retrieved 16 July 2007.
  40. ^ Phillips K (2007). "Feature Story: Viral Hemorrhagic Septicemia: A New Invader in the Great Lakes" (PDF). Fish Lines. 5 (5). Archived from the original (PDF) on 26 September 2007. Retrieved 16 July 2007.
  41. ^ Boomgaard J (9 January 2007). "New fish virus could be a little as 2 years away from Lake Michigan". Ludington Daily News. Archived from the original on 27 September 2007. Retrieved 13 July 2007.
  42. ^ Eckert M (26 January 2007). "Great Lakes Article: VHS disease has entered Great Lakes". Port Huron Times-Herald. Archived from the original on 27 September 2007.
  43. ^ Woo P (ed.). "Viral Haemorrhagic Septicaemia". WikiVet. Retrieved 11 October 2011.
  44. ^ a b Groocock GH (2007). "Viral Hemorrhagic Septicemia and Spring Viremia of Carp: Threats to Aquaculture" (PDF). Cornell University, College of Veterinary Medicine, Department of Microbiology and Immunology, Aquatic Animal Health Program. Archived from the original (PDF) on 7 June 2007. Retrieved 18 July 2007.
  45. ^ "Great Lakes fish hatcheries could benefit from new test for deadly VHS virus | Great Lakes Echo". 18 June 2009.
  46. ^ "Michigan vs the VHS virus" (PDF). Michigan Lakes & Streams Association, Inc. Archived from the original (PDF) on 18 February 2012.
  47. ^ Im J, Kim WR, Lee HE, Kim A, Kim DH, Choi YH, et al. (January 2020). "Expression analysis of LTR-derived miR-1269a and target gene, KSR2 in Sebastes schlegelii". Genes & Genomics. 42 (1): 55–65. doi:10.1016/j.fsi.2019.06.015. PMID 31721105. S2CID 195760294.
  48. ^ Ortega-Villaizan MD, Chico V, Perez L (July 2022). "Fish Innate Immune Response to Viral Infection-An Overview of Five Major Antiviral Genes". Viruses. 14 (7): 1546. doi:10.3390/v14071546. PMC 9317989. PMID 35891526.
[edit]
Retrieved from "https://en.wikipedia.org/w/index.php?title=Viral_hemorrhagic_septicemia&oldid=1259787959"